The genomics of rapid climatic adaptation and parallel evolution in North American house mice

Abstract

Parallel changes in genotype and phenotype in response to similar selection pressures in different populations provide compelling evidence of adaptation. House mice (Mus musculus domesticus) have recently colonized North America and are found in a wide range of environments. Here we measure phenotypic and genotypic differentiation among house mice from five populations sampled across 21° of latitude in western North America, and we compare our results to a parallel latitudinal cline in eastern North America. First, we show that mice are genetically differentiated between transects, indicating that they have independently colonized similar environments in eastern and western North America. Next, we find genetically-based differences in body weight and nest building behavior between mice from the ends of the western transect which mirror differences seen in the eastern transect, demonstrating parallel phenotypic change. We then conduct genome-wide scans for selection and a genome-wide association study to identify targets of selection and candidate genes for body weight. We find some genomic signatures that are unique to each transect, indicating population-specific responses to selection. However, there is significant overlap between genes under selection in eastern and western house mouse transects, providing evidence of parallel genetic evolution in response to similar selection pressures across North America. Dissecting the genetic basis of parallel evolution, the independent evolution of similar phenotypes in similar environments among closely related lineages, allows evolutionary biologists to test whether evolution is predictable at the molecular level. Relatively little is still known about the genetics of parallel evolution in quantitative traits. Here we identify significant phenotypic and genomic parallel evolution in quantitative traits across two latitudinal transects of wild house mice in eastern and western North America. We find parallel evolution in thermally adaptive phenotypes (nest building behavior and body mass) and in genes involved in temperature-related traits such as body mass, metabolism, and temperature-sensing using population genomic scans for selection. We also find considerable divergent phenotypic and genomic evolution between eastern and western transects corresponding to known environmental differences between these transects. In this case, the evolution of quantitative traits across similar latitudinal transects involved a mixture of unique and shared responses to selection at the molecular level.